Nuclear transport of baculovirus: Revealing the nuclear pore complex passage

Au, Shelly; Panté, Nelly

doi:10.1016/j.jsb.2011.11.006

Cited by 45 publications

(48 citation statements)

References 66 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…In this proposed mechanism the actin comet tail formed at one end of the nucleocapsid pushes the nucleocapsid through the NPC for nuclear import. In agreement with this model, the nucleocapsid crosses the NPC lengthwise with the end containing the actin-assembly-inducing VP78/83 protein away from the NPC (Au and Pante, 2012). Our model implies that the phenylalanine-glycine-rich nucleoporin (FG-Nup) permeability barrier at the NPC central channel can be breached by the propulsive force of actin polymerization.…”

Section: Nuclear Import Of Acmnpv Nucleocapsids In Digitoninpermeabilsupporting

confidence: 73%

“…AcMNPV nucleocapsids and VP39-3×mCherry nucleocapsids were obtained by de-enveloping the virus by treatment with 1% NP40 for 1 h at 30°C as described previously (Au et al, 2010;Au and Pante, 2012).…”

Section: Virus Nucleocapsid and Cy3-nls-bsamentioning

confidence: 99%

“…VP78/83 is a nucleation-promoting factor that activates actin polymerization by the host Arp2/3 complex (Goley et al, 2006). The rod-shaped nucleocapsid (30×250-300 nm) then enters the nucleus by crossing the NPC lengthwise (Au and Pante, 2012;Au et al, 2013). Whether baculoviruses use a conventional or an unconventional nuclear import pathway remains to be determined.…”

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

A new mechanism for nuclear import by actin-based propulsion used by a baculovirus nucleocapsid

Zhou

et al. 2016

Journal of Cell Science

Self Cite

View full text Add to dashboard Cite

The transport of macromolecules into the nucleus is mediated by soluble cellular receptors of the importin β superfamily and requires the Ran-GTPase cycle. Several studies have provided evidence that there are exceptions to this canonical nuclear import pathway. Here, we report a new unconventional nuclear import mechanism exploited by the baculovirus Autographa californica multiple nucleopolyhedrovirus (AcMNPV). We found that AcMNPV nucleocapsids entered the nucleus of digitonin-permeabilized cells in the absence of exogenous cytosol or under conditions that blocked the Ran-GTPase cycle. AcMNPV contains a protein that activates the Arp2/3 complex and induces actin polymerization at one end of the rod-shaped nucleocapsid. We show that inhibitors of Arp2/3 blocked nuclear import of nucleocapsids in semi-permeabilized cells. Nuclear import of nucleocapsids was also reconstituted in purified nuclei supplemented with G-actin and Arp2/3 under actin polymerization conditions. Thus, we propose that actin polymerization drives not only migration of baculovirus through the cytoplasm but also pushes the nucleocapsid through the nuclear pore complex to enter the cell nucleus. Our findings point to a very distinct role of actin-based motility during the baculovirus infection cycle.

show abstract

Section: Nuclear Import Of Acmnpv Nucleocapsids In Digitoninpermeabilsupporting

confidence: 73%

Section: Virus Nucleocapsid and Cy3-nls-bsamentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

A new mechanism for nuclear import by actin-based propulsion used by a baculovirus nucleocapsid

Zhou

et al. 2016

Journal of Cell Science

Self Cite

View full text Add to dashboard Cite

show abstract

“…The most abundant component of the nucleocapsids, which are typically 40 by 250 to 300 nm (3), is the VP39 protein (4,5). VP39 monomers assemble in the nuclei of infected cells into oligomeric ring-like structures, which are further folded into capsid tubules, likely with the help of the host actin cytoskeleton (6,7).…”

mentioning

confidence: 99%

Baculovirus VP1054 Is an Acquired Cellular PURα, a Nucleic Acid-Binding Protein Specific for GGN Repeats

Marek

Romier

Galibert

et al. 2013

J Virol

View full text Add to dashboard Cite

c Baculovirus VP1054 protein is a structural component of both of the virion types budded virus (BV) and occlusion-derived virus (ODV), but its exact role in virion morphogenesis is poorly defined. In this paper, we reveal sequence and functional similarity between the baculovirus protein VP1054 and the cellular purine-rich element binding protein PUR-alpha (PUR␣). The data strongly suggest that gene transfer has occurred from a host to an ancestral baculovirus. Deletion of the Autographa californica multiple nucleopolyhedrovirus (AcMNPV) vp1054 gene completely prevented viral cell-to-cell spread. Electron microscopy data showed that assembly of progeny nucleocapsids is dramatically reduced in the absence of VP1054. More precisely, VP1054 is required for proper viral DNA encapsidation, as deduced from the formation of numerous electron-lucent capsid-like tubules. Complementary searching identified the presence of genetic elements composed of repeated GGN trinucleotide motifs in baculovirus genomes, the target sequence for PUR␣ proteins. Interestingly, these GGN-rich sequences are disproportionally distributed in baculoviral genomes and mostly occurred in proximity to the gene for the major occlusion body protein polyhedrin. We further demonstrate that the VP1054 protein specifically recognizes these GGN-rich islands, which at the same time encode crucial proline-rich domains in p78/83, an essential gene adjacent to the polyhedrin gene in the AcMNPV genome. While some viruses, like human immunodeficiency virus type 1 (HIV-1) and human JC virus (JCV), utilize host PUR␣ protein, baculoviruses encode the PUR␣-like protein VP1054, which is crucial for viral progeny production.

show abstract

“…Viral structural proteins and genomic DNA assemble to produce nucleocapsids in the virogenic stroma in the nucleus (6). Initially, nucleocapsids egress primarily through the nuclear pore complexes to the cytoplasm and acquire an envelope from the plasma membrane to bud out to produce BV (7,8). In contrast, nucleocapsids destined to remain in the nucleus acquire an envelope from blebbing of the inner nuclear membrane (INM) to form ODVs (8,9).…”

mentioning

confidence: 99%

Baculovirus FP25K Localization: Role of the Coiled-Coil Domain

Garretson

McCoy

Cheng

2016

J Virol

View full text Add to dashboard Cite

Two types of viruses are produced during the baculovirus life cycle: budded virus (BV) and occlusion-derived virus (ODV). A particular baculovirus protein, FP25K, is involved in the switch from BV to ODV production. Previously, FP25K from the model alphabaculovirus Autographa californica multiple nucleopolyhedrovirus (AcMNPV) was shown to traffic ODV envelope proteins. However, FP25K localization and the domains involved are inconclusive. Here we used a quantitative approach to study FP25K subcellular localization during infection using an AcMNPV bacmid virus that produces a functional AcMNPV FP25K-green fluorescent protein (GFP) fusion protein. During cell infection, FP25K-GFP localized primarily to the cytoplasm, particularly amorphous structures, with a small fraction being localized in the nucleus. To investigate the sequences involved in FP25K localization, an alignment of baculovirus FP25K sequences revealed that the N-terminal putative coiled-coil domain is present in all alphabaculoviruses but absent in betabaculoviruses. Structural prediction indicated a strong relatedness of AcMNPV FP25K to long interspersed element 1 (LINE-1) open reading frame 1 protein (ORF1p), which contains an N-terminal coiled-coil domain responsible for cytoplasmic retention. Point mutations and deletions of this domain lead to a change in AcMNPV FP25K localization from cytoplasmic to nuclear. The coiled-coil and C-terminal deletion viruses increased BV production. Furthermore, a betabaculovirus FP25K protein lacking this N-terminal coiled-coil domain localized predominantly to the nucleus and exhibited increased BV production. These data suggest that the acquisition of this N-terminal coiled-coil domain in FP25K is important for the evolution of alphabaculoviruses. Moreover, with the divergence of preocclusion nuclear membrane breakdown in betabaculoviruses and membrane integrity in alphabaculoviruses, this domain represents an alphabaculovirus adaptation for nuclear trafficking of occlusion-associated proteins. IMPORTANCEBaculovirus infection produces two forms of viruses: BV and ODV. Manufacturing of ODV involves trafficking of envelope proteins to the inner nuclear membrane, mediated partly through the FP25K protein. Since FP25K is present in alpha-, beta-, and gammabaculoviruses, it is uncertain if this trafficking function is conserved. In this study, we looked at alpha-and betabaculovirus FP25K trafficking by its localization. Alphabaculovirus FP25K localized primarily to the cytoplasm, whereas betabaculovirus FP25K localized to the nucleus. We found that an N-terminal coiled-coil domain present in all alphabaculovirus FP25K proteins, but absent in betabaculovirus FP25K, was critical for alphabaculovirus FP25K cytoplasmic localization. We believe that this represents an evolutionary process that partly led to the gain of function of this N-terminal coiled-coil domain in alphabaculovirus FP25K to aid in nuclear trafficking of occlusion-associated proteins. Due to betabaculovirus breakdown of the nuclear membrane be...

show abstract

Nuclear transport of baculovirus: Revealing the nuclear pore complex passage

Cited by 45 publications

References 66 publications

A new mechanism for nuclear import by actin-based propulsion used by a baculovirus nucleocapsid

A new mechanism for nuclear import by actin-based propulsion used by a baculovirus nucleocapsid

Baculovirus VP1054 Is an Acquired Cellular PURα, a Nucleic Acid-Binding Protein Specific for GGN Repeats

Baculovirus FP25K Localization: Role of the Coiled-Coil Domain

Contact Info

Product

Resources

About